Cytogenetic studies in the redtail catfish, Phractocephalus hemioliopterus (Bloch & Schneider, 1801) (Siluriformes, Pimelodidae) a giant fish from Amazon basin

CompCytogen I 1(1): 119-128 (2017) COMPARATIVE *reevrervedorenacessiours

doi: 10.3897/CompCytogen.v! lil. 1152 Kan Cyto genetics

http://compcytogen.pensoft.net International journal of Plant & Animal Cytogenetics,

Karyosystematics, and Molecular Systematics

Cytogenetic studies in the redtail catfish,
Phractocephalus hemioliopterus (Bloch &

Schneider, 1801) (Siluriformes, Pimelodidae)
a giant fish from Amazon basin

Ana Claudia Swarga', Ana Lucia Dias’, Alberto Sergio Fenocchio?

| Departamento de Histologia, CCB, Universidade Estadual de Londrina. 86051-970, Caixa Postal 6001,
Londrina, Parand, Brazil2. Departamento de Biologia Geral, CCB, Universidade Estadual de Londrina, Caixa
Postal 6001, Londrina, Paranda, Brazil 3 Departamento de Genética, Universidad Nacional de Misiones. In-
stituto de Biologta Subtropical (IBS UNaM-CONICET). Félix de Azara 1552. 3300, Posadas, Misiones,
Argentina

Corresponding author: Ana Claudia Swarca (swarca@uel.br)

Academic editor: E. Gornung | Received 10 November 2016 | Accepted 5 January 2017 | Published 6 March 2017
http://zoobank. ore!74B0 DFE0-8 CB8-43FC-8867-5OCCBCE985B3

Citation: Swarca AC, Dias AL, Fenocchio AS (2017) Cytogenetic studies in the redtail catfish, Phractocephalus
hemioliopterus (Bloch & Schneider, 1801) (Siluriformes, Pimelodidae) a giant fish from Amazon basin. Comparative
Cytogenetics 11(1): 119-128. https://doi.org/10.3897/CompCytogen.v1 1i1.11152

Abstract

The objective of this study was to cytogenetically analyze Phractocephalus hemioliopterus comparing the
findings with other data to infer relationships among Pimelodidae species. The results revealed a diploid
number of 2n = 56 and the karyotype composed of 16 metacentric, 20 submetacentric, 6 subtelocentric
and 14 acrocentric chromosomes (FN = 98). The Ag-NORs, 18S rDNA and CMA, signals were coincident
in location occupying the short arm of an acrocentric chromosome pair (23"), in a secondary constriction.
The 5S rDNA genes were localized near the centromere on the short arms of one submetacentric chromo-
some pair. C-bands were localized predominantly in the terminal regions of chromosomes, including the
AgNORs and a small metacentric pair with a conspicuous positive band on interstitial region. This chro-

mosome pair could be considered a species-specific cytogenetic marker.

Keywords
Neotropical fish, Parrot catfish, karyotype, Ag-NORs, 18S rDNA, CMA,, C-banding

Copyright Ana Claudia Swarca et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC
BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

120 Ana Claudia Swarca et al. / Comparative Cytogenetics 11(1): 119-128 (2017)

Introduction

The genus Phractocephalus Agassiz, 1829 belongs to Pimelodidae family and contains
three species, one extant, Phractocephalus hemioliopterus (Bloch & Schneider, 1801)
and two extinct species recently described, P. nassi (Lundberg and Aguilera, 2003) and
P. acreornatus (Aguilera et al. 2008). According to Lundberg et al. (1998) “isolation of
peripheral drainage system south, west and north of the Parana, Amazonas and Orino-
co systems provided opportunity for allopatric divergence, and also was accompanied
by much extirpation of once more widespread tropical fish species”.

The large catfish, P. hemioliopterus, has a wide distribution in the lowland, mean-
dering rivers and lagoons of the Orinoco, Amazon and Essequibo (Lundberg and Agu-
ilera 2003) and as a monotypic taxon possesses several uniquely derived characteristics
(de Pinna 1998). This catfish is known as “cajaro” in Venezuela and Colombia and in
Brazil as “pirarara” (parrot — fish) because of its red or orange caudal fin (Lundberg and
Aguilera 2003). In the areas of occurrence, the species has economic importance and
is much appreciated by fishermen. However, in spite of its large size, Phractocephalus is
also a common aquarium fish (Carvalho and Medeiros 2005).

From a systematic point of view, Pimelodidae remains as a controversial group, pos-
sessing some internal inconsistencies, represented by the “Pimelodus group”, “Calophysus
group” and a basal branch including three genera Phractocephalus, Leiarius Bleeker,
1862 and Perrunichthys Schultz, 1944 (Lundberg and Littman 2003).

Available cytogenetic data partially support this hypothesis because several chro-
mosomal studies on Pimelodidae have revealed that the species of this family have a
predominant diploid number of 56 (Table 1) with a few exceptions, such as species
included in the “Calophysus group” that show some characteristic cytogenetic features
as 2n = 50, reported in Calophysus Miller & Trosche, 1843, Luciopimelodus Eigen-
mann & Eigenmann, 1888 and Pinirampus Bleeker, 1858 (Ramirez-Gil et al. 1998,
Swarc¢a et al. 1999, Sanchez et al. 2010) and Megalonema platanum (Ginther, 1880)
with 2n = 54 (Carvalho et al. 2011). According to phylogenetic tree of Lundberg and
Littman (2003) the branch that includes Leiarius, Perrunichthys and Phractocephalus has
been never studied cytogenetically; this fact demonstrates that more species must be
chromosomally studied to increase the number of cytogenetic data to better understand
the species relationships and the karyotypic evolution in this fish group. The present
work aims to report for the first time the cytogenetic study of P. hemioliopterus, a unique
extant species of the genus Phractocephalus from the Amazon Basin.

Material and methods

Six specimens of P hemioliopterus from Amazon Basin/Brazil maintained in the fishing
farm of the Universidade Estadual de Londrina were studied cytogenetically. The chro-
mosome preparations were obtained from lymphocyte culture according to Fenoc-
chio and Bertollo (1988), avoiding the sacrifice of specimens. Silver staining of NORs

Cytogenetic studies in the redtail catfish, Phractocephalus hemioliopterus... A 2A

Table |. Cytogenetic data on the family Pimelodidae. 2n = diploid number. Only published data were used.

2n References
“Pimelodus group”
as ee es 56 Dias and Foresti (1993)
Inetbietchias Bisco Carvalho et al. (2004); Carvalho and Dias (2005); Carvalho
Norris, 1900 56 et al. (2010); Vissotto et al. (1999); Ribeiro et al. (2008);
: Sanchez et al. (2014)
Parapimelodus La Monte, 1933 56 Treco et al., 2008.
Schell (1973); Toledo and Ferrari (1976); Dias and Foresti
ie a (1993); Vissotto et al. (1999); Swarga et al. (2001b); Borin and
Pimelodus Lacepéde, 1803 56 Martins-Santos (2002); Souza et al. (2003); Borin and Martins-
Santos (2004); Souza et al. (2004a, b); Garcia and Moreira Filho
(2005); Treco and Dias (2009); Moraes-Neto et al. (2011)
“Calophysus group”
oe Peru ener slrosenel 50 Ramirez-Gil et al. (1998)
Pinirampus Bleeker 1858 50 Swarga et al. (1999); Sanchez et al. (2010)
er ? 50 Sanchez et al. (2010)
“Megalonema group”
Megalonema Eigenmann, 1912 54 Carvalho et al. (2011)
“Sorubiminae group’
Hemisorubim Bleeker, 1862 56 Martins-Santos et al. (1996); Swarca et al. (2013)
Fenocchio and Bertollo (1992); Martins-Santos et al. (1996);
Pseudoplatystoma Bleeker, 1862 56 Swarga et al. (2005b), Moraes-Neto et al. (2011);
Nirchio el al. (2013)
Zungaro Bleeker, 1858 56 Martins-Santos et al. (1996); Swarca et al. (2001c)

; Fenocchio and Bertollo (1992); Martins-Santos et al. (1996);
Sorubim Cuvier, 1829 56 ieee etal. 2011 ( )
Brachyplatystoma Bleeker, 1862 56 Gongalves et al. (2014)

Steindachneridion Eigenmann & 56 Swarga et al. (2005a); Swarca et al. (2006);
Eigenmann, 1919 Moraes-Neto et al. (2011)
Phractocephalus Agassiz, 1829 56 Present data

(AgNORs) was performed using the method of Howell and Black (1980). C banding
and Chromomycin A, (CMA,) staining were carried out using the methods of Sumner
(1972) and Verma and Babu (1995), respectively. Fluorescence in situ hybridization
(FISH) experiments were performed using biotinylated 18S rDNA probes (1700 bp
fragments) obtained from the nuclear DNA of the fish Oreochromis niloticus (Linnaeus,
1758) labeled with biotin-14-dATP by nick translation (Gibco cat N° 18247-015), ac-
cording to the manufacturer's instructions. The hybridization technique, post-hybrid-
ization washes and visualization were carried out following Swarga et al. (2001c). The
preparations were analyzed in an Olympus BX50 microscope, and the best metaphases
were captured with a SONY camera, model Exware HAD coupled to the microscope.
The FISH slides were observed and the images acquired with a Leica DM 4500 mi-

122 Ana Claudia Swarca et al. / Comparative Cytogenetics 11(1): 119-128 (2017)

croscope equipped with a DFC 300F9 camera and Leica IM50 4.0 software. Chro-
mosome morphology was determined on the basis of Levan et al. (1964) and Guerra
(1986) with some modifications and chromosomes were classified as metacentric (m),
submetacentric (sm), subtelocentric (st) and acrocentric (a). NF (chromosome arm
number) was determined considering m/sm/st chromosomes having two arms and
acrocentric chromosomes having one arm.

Results and discussion

The family Pimelodidae is composed of 109 valid species (Eschmeyer and Fong 2016),
but only 27 species have been analyzed cytogenetically (Swarca et al. 2007). Phracto-
cephalus is a monotypic genus. The only species of the genus, P hemioliopterus, is wide-
ly distributed in the rivers of the Orinoco, Amazon and Essequibo basins (Lundberg
and Aguilera 2003). ‘The extinction of the other two species (P nassi and P acreornatus)
was hypothetically explained by Lundberg et al. (1998).

The diploid number (2n = 56) and karyotype constitution, 16m, 20sm, 6st, 14a
(FN = 98) of P. hemioliopterus is reported for the first time (Fig. 1). According to Swar-
ca et al. (2000) the chromosome number is identical to other large species that belong
to the “Pimelodus group” comprising at least Hemisorubim Bleeker, 1862, Zungaro
Bleeker, 1858, Sorubim Cuvier, 1829, Pseudoplatystoma Bleeker, 1862 that could be
called informally “Sorubiminae group” and includes the largest catfishes from South
America (de Pinna 1998, Lundberg and Littman 2003) (Table 1). Although P. 4e-
mioliopterus does not belong to these systematic and/or taxonomic groups, this species
shares many cytogentic traits, such as the chromosome shape, size and staining pat-
terns, with the species included in “Sorubiminae”.

As stated below, diploid number 56 with high fundamental number, NORs lo-
cated at the terminal position on the short arm of an acrocentric chromosome pair
(23), coincident with positive C-bands (Fig. 2a) represent common features in al-
most all pimelodid species analyzed so far, suggesting that these cytogenetic traits were
conserved during the karyotype evolution and may have an ancient common origin
(Sanchez et al. 2010). The presence of ribosomal genes on the short arm of one st/a
chromosome pair is coincident with the location observed in the “Calophysus group”
(Sanchez et al. 2010) and “Sorubiminae group” (Swarga et al. 2008) and differs from
the “Pimelodus group”, where the ribosomal genes are located almost exclusively on the
long arm of m/sm chromosome pairs (Swarga et al. 2007).

The data obtained with CMA, indicate that the Ag-NORs of P. hemioliopterus are
rich in GC pairs (Fig. 2b), a general pattern also found in the family Pimelodidae by
several authors (Swarca et al. 2001a, b, c, Garcia and Moreira-Filho 2005, Swarca et
al. 2005b, Nirchio et al. 2013, among others). However, the exact location of ribo-
somal genes on chromosomes could be revealed exclusively by means of in situ hy-
bridization using 18S and 5S rDNA probes. After application of this procedure these
regions showed bright signals on short arms of one subtelocentric pair (18S rDNA

Cytogenetic studies in the redtail catfish, Phractocephalus hemioliopterus... 123

"AS RAMEN MX AK RA Ma on
1 2 3 4 5 6 T 8

sm| RA BA GA AA BEA AA AA BA GE

9 10 11 12 13 14 15 16 17 18

si AMAA AA
19 20 21

al ia AH AA OR wee AB oom

22 23 24 25 26 27 28 —

Figure |. Karyotype of Phractocephalus hemioliopterus. Conventional Giemsa staining. Scale bar: 5 um.

Figure 2. Metaphases of Phractocephalus hemioliopterus. a AgNO, staining b CMA, banding ¢ FISH
with 18S rDNA probe and d FISH with 5S rDNA probe. Arrows indicate the NOR-bearing chromo-

somes and arrowheads indicate the chromosome pair with 5S rDNA.

probe) and on short arms of another submetacentric chromosome pair (5S rDNA
probe) (Fig. 2c, d). In general, the 18S and 5S rDNA sites are not syntenic but located
on different chromosome pairs, this feature being the most frequent patter in several
Pimelodidae species (Carvalho et al. 2010, Swarca et al. 2008, 2009). However, re-
cently syntenic localization of the major rDNA clusters and the 5S sites were reported
in other species (Ziemniczak et al. 2012, Konerat et al. 2014, da Rocha et al. 2016).
So far, both patterns of rDNA and 5S rDNA localization, syntenic and not syntenic,

124 Ana Claudia Swarca et al. / Comparative Cytogenetics 11(1): 119-128 (2017)

Figure 3. Somatic metaphase of Phractocephalus hemioliopterus after C-banding. Arrowheads indicate the
chromosome pair with interstitial heterochromatin; arrows indicate the NOR-bearing chromosome and

asterisks indicate the chromosomes with heterochromatin blocks in both terminal regions.

have been described in Pimelodidae. Still, the evolutionary trend of ribosomal genes
chromosome distribution has not been yet outlined.

Heterochromatin distribution revealed by C-banding was evidenced on telomeric
regions of some chromosomes, one pair with bitelomeric bands and in the secondary
constriction on the short arm of NOR bearing pair (Fig.3). This last feature represents a
common trait shared by most pimelodids. Another interesting cytogenetic characteristic
is the presence of a small metacentric pair that shows a conspicuous heterochromatic
block in interstitial region (Fig. 3). Heterochromatin interstitially located has been re-
ported in some species of the family Pimelodidae, such as Pseudoplatystoma tigrinum
(Valenciennes, 1840) (Fenocchio and Bertollo 1992), Hemisorubim platyrhynchos (Va-
lenciennes, 1840) (Martins-Santos et al. 1996), Lheringichthys labrosus (Liitken, 1874)
(Vissotto et al. 1999) and also in species of the genus Pimelodus Lacépéde, 1803 (Treco
et al. 2008). The interstitial localization of a strong C-band in P. hemioliopterus on a small
metacentric chromosome can be a species-specific cytogenetic marker and could be use-
ful for future studies on the internal relationships of the species included in this group.

Taking into consideration the findings described previously, the present work is
the first to provide cytogenetic information about P. hemioliopterus.

The cytogenetic description of P. hemioliopterus allowed the karyotypic charac-
terization and the comparison of certain cytogenetic features shared in general with
other Pimelodidae, however, some of these traits distinguish the “Sorubiminae group”,
suggesting that this species could be integrated into the branch of the great catfishes.

Cytogenetic studies in the redtail catfish, Phractocephalus hemioliopterus... 125

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